微生物学报

Fungus	Function	References
Sclerotinia sclerotiorum	Mycelial and sclerotium development, pathogenicity	[55]
Fusarium fujikuroi	Mycelial development, conidia and carotenoids production	[56]
Fusarium proliferatum	Mycelial and sclerotium development, pathogenicity	[57]
Fusarium verticillioides	Mycelial and sclerotium development, pathogenicity, coercion tolerance	[58]
Metarhizium acridum	Mycelial development, pathogenicity, coercion tolerance	[16]
Beauveria bassiana	Mycelial development, conidia production, pathogenicity, coercion tolerance	[59]
Aspergillus flavus	Mycelial development, conidia, sclerotium and toxin production, pathogenicity, coercion tolerance	[60]
Penicillium digitatum	Mycelial development, conidial production and germination, pathogenicity	[61]
Colletotrichum higginsianum	Mycelial development, conidia production, pathogenicity, coercion tolerance	[62]

Fungus	Function	References
Sclerotinia sclerotiorum	Mycelial and sclerotium development, pathogenicity	[55]
Fusarium fujikuroi	Mycelial development, conidia and carotenoids production	[56]
Fusarium proliferatum	Mycelial and sclerotium development, pathogenicity	[57]
Fusarium verticillioides	Mycelial and sclerotium development, pathogenicity, coercion tolerance	[58]
Metarhizium acridum	Mycelial development, pathogenicity, coercion tolerance	[16]
Beauveria bassiana	Mycelial development, conidia production, pathogenicity, coercion tolerance	[59]
Aspergillus flavus	Mycelial development, conidia, sclerotium and toxin production, pathogenicity, coercion tolerance	[60]
Penicillium digitatum	Mycelial development, conidial production and germination, pathogenicity	[61]
Colletotrichum higginsianum	Mycelial development, conidia production, pathogenicity, coercion tolerance	[62]

Fungus	PKA	Function	References
Sclerotinia sclerotiorum	SsPKA	Mycelial development, pathogenicity, autophagy	[63]
SsPKAR	Mycelial development, pathogenicity, autophagy, infection cushion and sclerotium formation
Fusarium fujikuroi	FfPKA1	Mycelial development, bicarbacin prodcution	[64]
FfPKA2	Mycelial development, gibberellin (GA) synthesis
Fusarium verticillioides	CPK1	Mycelial development, conidia production, pathogenicity	[65]
Colletotrichum trifolii-alfalfa	Ct-PKAC	Mycelial development, conidia production, infection cushion formation, pathogenicity, coercion tolerance	[66]
Colletotrichum orbiculare-cucumber	Co-Rpk1	Mycelial development, conidia production, pathogenicity	[67]
Co-Cpk1	Conidia germination, infection cushion function, pathogenicity
Colletotrichum gloeosporioides-mango	Cg-PKAC	Conidia production, infection cushion function, pathogenicity	[68]
Colletotrichum higginsianum-Arabidopsis	Ch-PKA1	Mycelial development, conidia production, infection cushion formation, stress response, pathogenicity	[69]

Fungus	PKA	Function	References
Sclerotinia sclerotiorum	SsPKA	Mycelial development, pathogenicity, autophagy	[63]
SsPKAR	Mycelial development, pathogenicity, autophagy, infection cushion and sclerotium formation
Fusarium fujikuroi	FfPKA1	Mycelial development, bicarbacin prodcution	[64]
FfPKA2	Mycelial development, gibberellin (GA) synthesis
Fusarium verticillioides	CPK1	Mycelial development, conidia production, pathogenicity	[65]
Colletotrichum trifolii-alfalfa	Ct-PKAC	Mycelial development, conidia production, infection cushion formation, pathogenicity, coercion tolerance	[66]
Colletotrichum orbiculare-cucumber	Co-Rpk1	Mycelial development, conidia production, pathogenicity	[67]
Co-Cpk1	Conidia germination, infection cushion function, pathogenicity
Colletotrichum gloeosporioides-mango	Cg-PKAC	Conidia production, infection cushion function, pathogenicity	[68]
Colletotrichum higginsianum-Arabidopsis	Ch-PKA1	Mycelial development, conidia production, infection cushion formation, stress response, pathogenicity	[69]

植物病原真菌环磷酸腺苷信号通路研究进展

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蔡云飞 , 应佳丽 , 叶友菊 , 文爽爽 , 钱仁卷 ^*

微生物学报 | 综述 2024,64(12): 4746-4759

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微生物学报 | 综述 2024, 64(12): 4746-4759

植物病原真菌环磷酸腺苷信号通路研究进展

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蔡云飞, 应佳丽, 叶友菊, 文爽爽, 钱仁卷^*

作者信息

浙江省亚热带作物研究所, 浙江温州 325005

Research progress of cAMP signaling pathway in phytopathogenic fungi

Yunfei CAI, Jiali YING, Youju YE, Shuangshuang WEN, Renjuan QIAN^*

Affiliations

Zhejiang Institute of Subtropical Crops, Wenzhou 325005, Zhejiang, China

出版时间: 2024-09-24 doi: 10.13343/j.cnki.wsxb.20240405

文章导航

摘要

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环磷酸腺苷(cyclic adenosine monophosphate, cAMP)是广泛存在于真核生物中的第二信使，其由腺苷酸环化酶(adenylate cyclase, AC)合成后，通过结合蛋白激酶A (protein kinase A, PKA)调控下游蛋白活性，从而参与植物病原真菌的生长发育、致病性(或致病力)、细胞壁完整性、环境胁迫响应及有性/无性生殖等方面的调控。本文介绍了植物病原真菌cAMP信号通路的信号转导及其与细胞中其他信号通路之间的交叉调控的相关研究进展，同时阐述了cAMP信号通路在植物病原真菌侵染过程中的重要作用。为今后以cAMP信号通路相关基因或蛋白作为靶点筛选抑制植物病原真菌的药物，以及利用cAMP信号通路对植物病原真菌生长发育及致病等相关调控机制进行病害防控提供了新的策略和思路。

关键词

植物病原真菌 / cAMP信号通路 / 致病力 / 腺苷酸环化酶

Abstract

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Cyclic adenosine monophosphate (cAMP) is a second messenger widely present in eukaryotes. It is synthesized by adenylate cyclase (AC) and regulates downstream protein activity by binding to protein kinase A, thereby regulating fungal growth and development, virulence, cell wall integrity, environmental stress responses, and sexual/asexual reproduction. This article introduces the research progress of the cAMP signaling pathway in phytopathogenic fungi and the cooperation of this pathway with other signaling pathways in regulating cellular processes. At the same time, it elucidates the role of the cAMP signaling pathway in the infection of plant phytopathogenic fungi. This review is expected to provide reference for screening the agents for inhibiting phytopathogenic fungi that target the genes or proteins in the cAMP pathway. Additionally, the cAMP signaling pathway could be targeted to prevent and control the growth, development, and pathogenicity of phytopathogenic fungi in the future.

Key words

phytopathogenic fungi / cAMP signaling pathway / pathogenicity / adenylate cyclase

引用本文

蔡云飞, 应佳丽, 叶友菊, 文爽爽, 钱仁卷. 植物病原真菌环磷酸腺苷信号通路研究进展. 微生物学报, 2024 , 64 (12) : 4746 -4759 . DOI: 10.13343/j.cnki.wsxb.20240405

Yunfei CAI, Jiali YING, Youju YE, Shuangshuang WEN, Renjuan QIAN. Research progress of cAMP signaling pathway in phytopathogenic fungi[J]. Acta Microbiologica Sinica, 2024 , 64 (12) : 4746 -4759 . DOI: 10.13343/j.cnki.wsxb.20240405

正文

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植物约70%−80%的病害是由植物病原真菌引起的^[1]，例如稻瘟菌(Magnaporthe oryzae)可引起水稻的稻瘟病，禾谷镰孢菌(Fusarium graminearum)可侵染众多禾谷类作物，灰葡萄孢(Botrytis cinerea)引起的灰霉病则是番茄、葡萄及草莓等众多园艺作物的常见病害^[2]。植物病原真菌由于寄主不同，其侵染策略也不尽相同，如可形成附着胞、侵染垫及侵染钉等不同侵染结构以侵染寄主^[3-4]，影响寄主的活性氧(reactive oxygen species, ROS)信号以侵染宿主^[4]，通过分泌毒素等次生代谢产物来辅助侵染寄主等^[4-5]。植物病原真菌的侵染策略多种多样，多数植物病原真菌可以通过空气、水流等媒介迅速传播^[6]，不同病害可能会同时发生，因此植物病害难以彻底防控。目前，农业生产中主要以化学药剂防治植物真菌病害，一方面会造成环境污染、土壤退化的问题，另一方面会导致植物病原真菌产生抗药性，从而使植物病原真菌更加难以防控^[7]。因此针对植物病原真菌的靶向药及新型绿色防控策略的研发迫在眉睫。

植物病原真菌的营养通常来源于寄主，因此病原真菌对外界环境的感知尤为重要。Butcher等于1965年首次提出细胞第二信使学说，将环磷酸腺苷(cyclic adenosine monophosphate, cAMP)称为仅次于激素的第二信使^[8]。病原真菌可以通过cAMP及其他第二信使介导的信号通路感知外界环境信号的变化，调整生存策略，从而更好地侵染宿主^[2]。cAMP信号通路是G蛋白偶联受体(G protein-coupled receptors, GPCRs)调控的下游重要信号通路之一^[9]，cAMP信号通路的调控机制如下：cAMP是腺嘌呤核苷三磷酸(adenosine triphosphate, ATP)在腺苷酸环化酶(adenylate cyclase, AC)的作用下合成，以GPCRs为代表的细胞膜感受器感知外界信号后，通过G蛋白调控AC的活性来影响胞内cAMP的浓度，而cAMP浓度的变化会影响与其结合的蛋白激酶A (protein kinase A, PKA)的活性，从而进一步影响下游转录因子及相关蛋白的磷酸化水平，最终使得细胞响应外界环境变化^[9]。除G蛋白外，大鼠肉瘤(rat sarcoma, RAS)等其他蛋白在接收到上游信号后也可以调控AC活性，并通过下游的PKA将多种外界刺激信号转变为均匀的胞内信号，调控细胞对外界刺激信号的响应^[10]。

cAMP信号通路是真核生物中非常保守的信号通路^[11]，本文以植物病原真菌中的灰葡萄孢、稻瘟菌及禾谷镰孢菌等为代表，总结植物病原真菌中cAMP信号通路相关组分、调控机制及相关信号通路间的交叉调控，以及cAMP信号通路对植物病原真菌的生长发育、致病力等方面的影响，为后续以cAMP信号通路的不同组分为筛选靶点，筛选防治植物病原真菌的特效靶向药，以及新型防控策略的研究提供科学依据。

1 植物病原真菌中cAMP信号的传导

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cAMP在细胞中由AC合成，GPCRs感受器在感知外界环境信号后，通过G蛋白异三聚体Gαβγ解离后活化的Gα亚基，调控AC合成cAMP。除G蛋白外，RAS蛋白、G蛋白信号调节因子(regulators of G protein signaling, RGS)类似蛋白(RGS-like proteins)以及环化酶相关蛋白1 (cyclase-associated protein 1, CAP1)等蛋白也可通过与AC互作调节其活性，催化ATP生成cAMP^[12]。

蛋白激酶PKA与磷酸二酯酶(phosphodiesterase, PDE)分别通过与cAMP结合后的激活或对cAMP的分解，实现对cAMP信号通路下游的调控。cAMP合成后，会结合蛋白激酶A调节亚基(PKA regulatory subunit, PKA-R)后释放活化的蛋白激酶A催化亚基(PKA control subunit, PKA-C)，活化的PKA-C以磷酸化其他蛋白或蛋白互作的形式调控下游的相关蛋白及转录因子活性，从而影响植物病原真菌的生长发育及致病力^[9]。cAMP在细胞内的扩散速度最快可以达到700 μm²/s，cAMP浓度的迅速变化会影响PKA对下游的调控，因此对cAMP在胞内不同位置的浓度进行控制十分重要^[13]。PDE可以降解cAMP来调控cAMP在胞内不同位置的浓度，以降低PKA活性，从而参与到cAMP信号通路的调控中，并调控真菌的生命活动(图1)^[14]。

2 cAMP信号通路对植物病原真菌生长发育及致病力的调控

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植物病原真菌侵染植物需要感知宿主，并突破宿主的细胞壁等物理屏障，因此不同的植物病原真菌特化出了不同的侵染结构和侵染策略，例如稻瘟菌会形成附着胞、侵染垫及侵染钉等不同侵染结构，从而实现植物病原真菌黏附、穿透宿主细胞的过程^[5]，以禾谷镰孢菌为代表的多种镰孢菌属成员则通过分泌脱氧雪腐镰孢菌烯醇(deoxynivalenol, DON)等毒素帮助侵染寄主^[15]，而灰葡萄孢可以形成附着胞及侵染垫等侵染结构，也可以合成博特西尼酸(botcinic acid, BOA)及葡双醛霉素(botrydial, BOT)毒素，是侵染策略比较复杂的植物病原真菌^[4]。

对不同植物病原真菌cAMP信号通路组分的缺失突变体研究表明，cAMP信号通路对植物病原真菌的生长发育及致病力至关重要^[9]。因此本文以农业生产中危害性大、传播度广、暴发速度快的几种常见植物病原真菌(稻瘟菌、禾谷镰孢菌、灰葡萄孢)为典型代表进行论述，介绍cAMP信号通路对植物病原真菌生长发育及致病力的影响，并对其他植物病原真菌中cAMP信号通路对生长发育及致病力的调控进行综述。

2.1 cAMP信号通路对稻瘟菌生长发育及致病力的调控

稻瘟菌是引起水稻等多种粮食作物稻瘟病的半活体型营养真菌(hemibiotroph)，其主要通过附着胞部分的巨大膨压形成侵染钉，刺破植物细胞壁完成侵染，因此附着胞的形成对其生长发育及致病力非常重要^[16]。对稻瘟菌合成cAMP的腺苷酸环化酶MAC1的研究表明，cAMP信号通路会参与稻瘟菌的生长发育、分生孢子的产生、附着胞的形成及致病力相关表型的调控^[16]。外源添加cAMP可以诱导稻瘟菌菌丝在非亲水表面附着胞的分化，部分恢复附着胞特异蛋白1 (appressorium memberane-specific protein, Pams1)缺失突变体的附着胞形成缺陷^[17-18]，并减弱温度对附着胞形成的影响^[19]。因此，cAMP信号通路参与稻瘟菌对寄主表面的识别以及侵染结构的形成，影响其生长发育及致病力。

真菌通过细胞膜表面的GPCRs来感知外界信号，并通过G蛋白对下游进行调控。稻瘟菌中组成G蛋白的Gαβγ异三聚体中，缺失Gα亚基或Gβ亚基后，其胞内的cAMP水平会降低，且附着胞减少、致病力下降^[20-21]；而Gγ亚基表达受到抑制后，稻瘟菌的无性/有性孢子形成、附着胞形成和致病力均受到影响，通过添加外源cAMP或PDE的抑制剂3-异丁基-1-甲基黄嘌呤(isobutylmethylxanthine, IBMX)，可部分恢复附着胞形成过程中的缺陷^[3]。RGS可以调控活化的Gα亚基使其失活，而稻瘟菌中的MoRgs7可以调控cAMP信号通路，从而参与附着胞的形成及致病力^[22]。RAS蛋白是除G蛋白外另一类可以直接调控AC活性的蛋白，Ras鸟嘌呤核苷酸交换因子(Ras guanine nucleotide exchange factors, RasGEFs)主要负责RAS蛋白的激活，稻瘟菌RasGEF蛋白MoCDC25的缺失会使得胞内cAMP含量降低，外源添加cAMP可部分回复突变体附着胞形成缺陷^[23]。另外，稻瘟菌中AC相关结合蛋白CAP1 (AC-associated and actin-binding protein CAP1)的缺失使得胞内cAMP水平降低，附着胞形态缺陷，并且致病力减弱^[24]。综上所述，稻瘟菌中AC上游的G蛋白、RGS蛋白及RAS蛋白均参与cAMP信号通路的调控。

AC合成cAMP后，PKA通过结合cAMP活化并发挥调控下游的功能。稻瘟菌中，PKA亚基的缺失影响了稻瘟菌的营养生长、无性生殖及附着胞的形成^[25]。真菌PDE主要通过降解cAMP参与调控cAMP信号通路，MoPdeH缺失后不仅可以影响细胞壁的完整性，其突变体孢子形态、表面疏水性感知等方面均出现缺陷^[26]。另外，Gβ类似活化蛋白激酶C1受体(Gβ-like/receptor for activated protein kinase C1, Gβlike/RACK1) MoMip11可以促进Gα蛋白MoMagA活化，抑制MoPdeH活性，从而上调细胞内cAMP水平^[27]。综上所述，结合cAMP的PKA与分解cAMP的PDE均参与稻瘟菌的生长发育及致病力，cAMP信号通路是参与稻瘟菌生长发育及致病力的重要信号通路之一。

2.2 cAMP信号通路对禾谷镰孢菌生长发育及致病力的调控

禾谷镰孢菌引起的小麦赤霉病是全球小麦生产的主要威胁^[28]。禾谷镰孢菌除了造成严重的产量损失以及谷物品质下降外，其在侵染谷物过程中还会产生DON、玉米赤霉烯酮(zearalenone, ZEA)毒素及其他次生代谢产物，危害人畜健康^[29-30]。对禾谷镰孢菌合成cAMP的腺苷酸环化酶FgAC1缺失突变体的研究表明，cAMP信号通路参与调控禾谷镰孢菌菌丝的生长发育、毒素合成、有性发育及致病力^[31]，其中腺苷酸环化酶Fac1、PKA催化亚基钙依赖性蛋白激酶1 (calcium-dependent protein kinases, CPK1)以及PKA调节亚基PKR的缺失突变体的菌丝生长发育、致病力均受到影响^[31-35]，PKA催化亚基CPK2缺失后无明显表型^[34-35]，表明CPK1是禾谷镰孢菌中的主要PKA。与CPK1及PKR不同，FgAC1的缺失对分生孢子形态无明显影响^[31]。

禾谷镰孢菌中DON的合成主要受双途径特异性转录因子(pathway-specific transcription factors) Tri6和Tri10的调控^[5]。外源cAMP处理可以诱导TRI家族基因表达以及DON相关的细胞分化(DON-associated cellular differentiation)，并部分恢复Tri10缺失突变体DON合成缺陷表型^[5]，Tri6缺失后与cAMP信号通路相关的几个组分的基因表达量也受到抑制^[32]，且禾谷镰孢菌的腺苷酸环化酶FgAC1突变后无法合成DON^[31]，以上研究表明cAMP信号通路与禾谷镰孢菌的DON毒素合成和致病力紧密相关。

禾谷镰孢菌中环化酶相关蛋白FgCAP1也参与了cAMP信号对DON合成的调控，而FgCAP1对DON的调控受到TRI6的反馈调节^[32]。RAS蛋白是调控cAMP信号通路的上游蛋白之一，禾谷镰孢菌中的RasGEF蛋白FgCdc25缺失后不能形成侵染结构，并且DON合成减少，外源添加cAMP可部分恢复其致病力^[33]。对CPK1及PKR的缺失突变体的研究表明，CPK1及PKR参与调控禾谷镰孢菌的营养生长、分生孢子的产生以及DON的合成，而CPK2的缺失未观察到明显的表型^[34-35]，表明cAMP信号通路主要通过CPK1及PKR调控DON的合成。另外，禾谷镰孢菌G蛋白偶联受体GIV1通过调控CPK1的活性参与侵染垫等侵染结构的形成^[36]，表明GIV1可能是调控cAMP信号通路的上游感受器。PDE可以通过分解cAMP调控PKA的活性，禾谷镰孢菌中PDE1及PDE2对禾谷镰孢菌的生长发育、分生孢子的形成及侵染寄主均有调控作用，但只有PDE2的缺失会激活PKA的活性并诱导DON的合成^[4]，这表明PDE2是禾谷镰孢菌中主要分解cAMP的磷酸二酯酶。综上所述，禾谷镰孢菌中CAP1及RAS等上游蛋白可通过调控cAMP信号通路参与调控DON合成，而PDE通过对cAMP的分解影响PKA相关组分的活性，从而参与禾谷镰孢菌DON的合成。

除DON毒素外，ZEA是另一种由镰孢菌属真菌合成的雌激素类真菌毒素。ZEA可以诱导哺乳动物的高雌激素效应，从而影响哺乳动物的生殖健康^[37]。cAMP信号通路可以抑制ZEA合成关键基因Zeb2L的表达，参与Zeb2L的转录后调控，从而负调控ZEA的合成^[38]。研究表明，cAMP信号通路还参与调控禾谷镰孢菌ZEA的合成。

2.3 cAMP信号通路对灰葡萄孢生长发育及致病力的调控

灰葡萄孢是一种典型的坏死营养型植物病原真菌，其具有寄主广泛、致病力强、侵染方式多样、防治困难等特点^[39]。由灰葡萄孢引起的灰霉病，对于葡萄、番茄等果蔬采前及采后有着非常大的危害^[39]。灰葡萄孢可以形成附着胞、侵染垫等侵染结构，也可以通过调控寄主ROS信号诱导寄主细胞死亡^[3]。对灰葡萄孢合成cAMP的腺苷酸环化酶BAC缺失突变体的研究表明，cAMP信号通路参与了灰葡萄孢生长发育、分生孢子的产生、菌核的产生、致病力及昼夜节律的调控^[39-40]，另外对BAC位于PP2C (type 2C serine/threonine phosphatases)结构域的S1407位点突变菌株的研究表明，S1407位点是磷酸化位点，并且该位点的突变影响了灰葡萄孢总蛋白中不同蛋白的磷酸化水平^[39]，暗示了BAC的PP2C结构域具有去蛋白磷酸化的功能。

番茄是灰霉菌的重要宿主之一，番茄的栽培过程中发生灰霉病可导致番茄产量减产60%以上。番茄灰霉病已经成为制约番茄设施栽培的主要真菌病害。番茄成熟过程中会释放挥发性有机化合物，其中的乙烯和苯甲醛可以结合G蛋白偶联受体BcGPR3并降低其活性，从而通过cAMP信号通路启动分生孢子的萌发^[41]，并且外源添加cAMP对Gαlll亚基Bcg3缺失突变体分生孢子萌发速率加快的表型有恢复作用^[42]，表明cAMP信号通路是灰葡萄孢识别寄主的重要信号通路。另外G蛋白β亚基Bcgb1的缺失使得胞内cAMP信号通路相关组分基因的表达量下降，胞内cAMP含量显著升高，表明G蛋白亚基Bcgb1也参与了cAMP信号通路的调控^[43]。

在灰葡萄孢中有PKA1和PKA2这2个PKA亚基，以及一个调节亚基PKA-R，其中PKA1和PKA-R缺失突变体与BAC缺失突变体的表型类似，均参与灰葡萄孢生长发育及致病力的调节^[44]。灰葡萄孢中有2个磷酸二酯酶BcPde1和BcPde2，其中BcPde2的缺失对灰葡萄孢的生长发育、菌核形成及毒素合成等有显著影响，而BcPde1的缺失无显著表型，且与其他真菌PDE缺失后cAMP水平上升不同，灰葡萄孢中BcPde1和BcPde2突变后胞内cAMP水平略微降低，且PKA的活性降低^{[42, 45]}，这可能暗示了灰葡萄孢的cAMP信号通路的调控方式与其他真菌有所不同。BcSDR1 (B. cinerea sclerotia deficient related 1)对灰葡萄孢的生长发育、分生孢子、菌核的形成及致病性有调控作用^[46]，通过使用RNA干扰技术研究表明，灰葡萄孢中BcPKA1和BcPKAR抑制BcSDR1表达，而BcPKA2可以正调控BcSDR1表达^[47]。综上所述，虽然灰葡萄孢的侵染手段多种多样，但cAMP信号是调控其生长发育及致病力的重要信号通路之一。

2.4 cAMP信号通路对其他植物病原真菌生长发育及致病力的调控

植物病原真菌种类众多，除稻瘟菌、禾谷镰孢菌及灰葡萄孢等植物病原真菌外，cAMP信号通路也广泛参与其他植物病原真菌的生长发育及致病力^[9]。炭疽菌(Colletotrichum spp.)是十字花科作物炭疽病的主要致病菌之一，希金斯炭疽菌(Colletotrichum higginsianum)的环化酶相关蛋白ChCAP缺失突变体的分生孢子形成、附着胞的形成及菌丝的生长速率等方面均受到抑制，外源cAMP可部分恢复ChCAP缺失突变体附着胞及细胞穿透方面的缺陷，表明cAMP信号通路参与调控炭疽菌的菌丝生长、附着体形成及致病力^[48]。甘蔗鞭黑粉菌(Sporisorium scitamineum)引起的甘蔗黑穗病会严重影响甘蔗的产量和品质，cAMP信号通路可以调控甘蔗鞭黑粉菌的活性氧水平，参与有性生殖及致病力的调控^[49]，另外甘蔗鞭黑粉菌的cAMP信号通路可以调控信息素响应转录因子Ssprf1的转录及胞内与寄主的活性氧信号，从而调控有性生殖及毒力^[50-51]。大丽轮枝菌(Verticillium dahliae)可潜伏在土壤中，通过侵染多种双子叶植物引发枯萎病，外源添加cAMP以及磷酸二酯酶VdPDEH的缺失可部分恢复玻璃纸表面诱导蛋白VdCSIN1缺失突变体的附着胞形成，表明cAMP信号通路参与大丽轮枝菌的致病过程^[52]。由稻曲病菌(Ustilaginoidea virens)引起的稻曲病是近年来全球范围广泛发生的水稻病害之一，其环腺苷相关蛋白UvCAP1的缺失菌株的菌丝生长、分生孢子的产生及致病力受到抑制，暗示了cAMP信号参与了稻曲病菌的生长发育及致病力^[53]。辣椒疫霉菌(Phytophthora capsici)的磷酸二酯酶PcPdeH对菌丝的营养生长、分生孢子萌发和致病性也至关重要^[54]。

另外，本文还列举了不同植物病原真菌AC (表1)及PKA (表2)的突变体表型，可以看到不同植物病原真菌AC突变后都影响其生长发育及致病力，表明cAMP信号通路在植物病原真菌中非常保守，且在侵染植物过程中发挥非常重要的功能。

3 植物病原真菌中cAMP信号通路与其他信号通路的交叉调控

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在真核生物中，不同的信号通路之间存在交叉及相互调节的现象，从而协同调控生物体的不同生理反应，真菌中存在类似的调控机制^[33]。对植物病原真菌的研究表明，cAMP信号通路会与雷帕霉素靶蛋白(target of rapamycin, TOR)、丝裂原活化蛋白激酶(mitogen-activated protein kinasse)等信号通路进行交叉调控，且TOR及MAPK信号通路与cAMP信号通路一样，也是真核生物中非常保守的信号通路，对植物病原真菌的研究表明TOR信号通路与MAPK信号通路同样广泛参与植物病原真菌的生长发育及致病力^{[9, 70-73]}。

TOR信号通路主要由雷帕霉素靶蛋白介导，雷帕霉素靶蛋白是真核生物中一种高度保守的丝氨酸/苏氨酸蛋白激酶^[74]。在稻瘟菌中，TOR信号通路通过对附着胞形成的调控影响其致病性^[74]。对稻瘟菌MAC1的研究表明，MAC1介导的cAMP信号通路可以通过激活TOR途径调控分生孢子萌芽管的生长，同时TOR途径的失活又可以负反馈调节Mac1的活性^[72]，并抑制cPKA活性以影响附着胞的形成^[73]。

MAPK信号通路同样是真核生物中非常保守的信号通路。大多数真菌包含3条MAPK信号通路，分别是与信息素响应相关的MAPK信号通路(Fus3/Kss1)、与细胞壁完整性相关的MAPK信号通路(Slt2)及与渗透相关的MAPK信号通路(Hog1)^[75]。MAPK信号通路广泛参与调控真菌中有性生殖结构的形成、菌丝侵染、细胞壁完整性及致病力等方面^[9]，其与cAMP信号通路类似，同样受到G蛋白及RAS蛋白的调控^[9]，例如灰葡萄孢中Gβ蛋白Bcgb1可通过cAMP及MAPK (Bmp1和Bmp3)信号通路调控灰葡萄孢的生长发育及致病力^[43]，禾谷镰孢菌中的Ras GTP酶FgCdc25通过cAMP及MAPK信号通路调控生长发育、DON合成及致病力^[33]。

对灰葡萄孢与渗透相关的MAPK信号通路Hog1同源蛋白BcSak1的缺失突变体的研究表明，BcSak1缺失后胞内cAMP含量显著上升，表明BcSak1对cAMP信号通路有调控作用^[69]。在稻瘟菌中，其磷酸二酯酶(PDE)可与参与细胞壁完整性相关的MAPK信号通路组分MoMck1互作，以调控细胞壁完整性^[70]，而PKA可以磷酸化转录因子MoSfl1，以调控菌丝生长发育，且PKA对MAPK信号通路组分Pmk1及Mps1的激活非常重要^[71]，表明在稻瘟菌中cAMP信号通路可以通过PKA调控MAPK信号通路的活性。在禾谷镰孢菌中，3条MAPK信号通路组分的缺失使得细胞内cAMP水平升高，表明MAPK信号通路可影响cAMP信号通路^[72-74]。另外，参与调控分生孢子形成及致病力的MAPK下游转录因子FgSfl1是cAMP和MAPK信号传导的共同靶标^[74]，表明在禾谷镰孢菌中cAMP信号通路与MAPK信号通路通过FgSfl1协同调控分生孢子的形成及致病力。在玉米黑粉菌中，cAMP信号通路与MAPK信号通路通过共同调控转录因子Prf1活性参与其有性生殖^[75]。以上研究表明，cAMP信号通路与MAPK信号通路之间具有非常复杂的交互作用，在上游受体、互作网络、下游靶基因等均有交叉调控。

植物病原真菌通过cAMP信号通路与其他信号通路之间的交叉调控，以调整菌丝的生长发育、致病力、有性及无性生殖结构的形成，不同信号通路之间的交叉调控使得植物病原真菌可以快速识别侵染寄主，快速适应外界环境变化并及时调整生存策略以适应环境。对cAMP与其他信号通路之间的交叉调控机制的研究可为防控植物病原真菌提供新的理论依据。

4 cAMP信号通路在植物病原真菌防控中的利用

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cAMP信号通路在真核生物中非常保守。在哺乳动物中，作为高度进化保守的cAMP途径中的关键酶，AC控制着细胞、组织、器官和生物体在健康和疾病中的生理机能^[76]，因此有许多以cAMP信号通路关键组分为靶点的药物。例如，在哺乳动物中可使用SQ22536抑制AC的活性^[77]，且可通过PKA抑制剂H89及PDE抑制剂IBMX正反调控cAMP信号通路^[78]。目前，以上cAMP信号通路抑制剂已在部分真菌中使用。SQ22536通过抑制AC活性以抑制cAMP信号通路，在灰葡萄孢中，SQ22536可抑制灰葡萄孢的菌丝生长发育^[47]。IBMX是哺乳动物中广泛使用的PDE抑制剂，在灰葡萄孢中使用IBMX可抑制其菌丝生长发育^[39]，在希金斯炭疽菌中使用IBMX则可以抑制其附着胞的形成^[79]，而在稻瘟病菌中，IBMX抑制菌丝的生长，虽然IBMX不会抑制其附着胞的形成，但可抑制其侵染钉的形成^[26]。

目前，虽然有研究证明了cAMP信号通路的相关抑制剂可以抑制植物病原真菌的生长发育及致病力，但在农业生产中还未有针对cAMP信号通路的农药以抑制植物病原真菌对农作物的侵染。cAMP信号通路作为真核生物中非常保守的信号通路，以cAMP信号通路组分作为药物靶点来抑制多种植物病原真菌的潜力巨大。

5 展望

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cAMP信号通路在植物病原真菌中非常保守，其广泛参与植物病原真菌的生长发育及致病性，且通过与其他信号通路交叉调控的方式响应外界环境变化，从而改变生存策略以适应目前及将来的环境变化。然而，目前对于植物病原真菌中cAMP信号通路与其他信号通路之间的交叉调控机制还不够完善，对于不同植物病原真菌cAMP信号通路下游的互作蛋白及相关转录因子有待进一步挖掘。cAMP信号通路是调控植物病原真菌生长发育及致病力的重要信号通路之一，对其与其他信号通路之间的交叉调控及其下游调控机制的发掘可能是cAMP信号通路未来的研究方向。

对植物病原真菌cAMP信号通路的研究表明，其与胞内的其他信号通路之间有不同程度的交叉。哺乳动物中AC可被HCO₃⁻及Ca²⁺直接激活，且AC对胞内ATP浓度变化比较敏感，AC也可以发挥CO₂/HCO₃⁻/pH敏感器的作用^[80]。目前对希金斯炭疽菌的研究暗示了Ca²⁺信号通路可能与cAMP信号通路有交叉调控^[81]，但对于这一领域的研究尚不够深入，在其他植物病原真菌中鲜有HCO₃⁻及Ca²⁺与cAMP信号通路间关系的相关研究。另外，真菌的AC包含人类及其他哺乳动物AC中所不具备的PP2C结构域，PP2C结构域属于Ser/Thr蛋白磷酸酶相关结构域中的一种，该类磷酸酶通过催化底物蛋白去除磷酸基团^[82]。灰葡萄孢的腺苷酸环化酶BAC的相关研究表明，BAC的S1407位点突变影响了其磷酸化水平，同时也影响了总蛋白中部分蛋白磷酸化水平^[39]。这暗示了BAC的PP2C结构域可能具有去蛋白磷酸化功能，然而，对于其他植物病原真菌中AC的PP2C结构域的具体功能，目前尚缺乏深入系统的研究。

cAMP信号通路在真核生物中非常保守，但在不同植物病原真菌中的功能同样存在一定的分化。例如cAMP信号通路在稻瘟菌中参与了附着胞的形成及对寄主的侵染；禾谷镰孢菌产生的毒素DON及ZEA等会危害人畜健康^[29-30]，cAMP信号通路与禾谷镰孢菌中DON及ZEA毒素的合成紧密相关^[31-35]；灰葡萄孢的侵染策略非常多样，既可以形成附着胞与侵染垫，也可以合成BOA及BOT等相关毒素辅助侵染^[3]，而cAMP信号通路组分的缺失显著影响了其致病力及毒素的合成^[39-40]。这些研究表明，在植物病原真菌的进化过程中，cAMP信号通路在保持对植物病原真菌生长发育的调控的同时，也在参与调控不同植物病原真菌侵染方式的分化。植物在生长过程中会同时面对多种植物病原真菌的威胁，cAMP信号通路的保守性使得在未来，面对不同植物病原真菌的防治过程中，可以使用针对cAMP信号通路的靶向药物同时抑制多种植物病原真菌的侵染，这可以为未来大田病害防治提供新的思路。

cAMP信号通路广泛参与植物病原真菌的生长发育、有性/无性生殖、次生代谢及致病性，植物病原真菌AC的缺失突变体的表型体现了cAMP信号通路对于植物病原真菌的重要性，在稻瘟菌、灰葡萄孢以及禾谷镰孢菌中的研究均印证了这一点。然而，一方面依然缺乏能将不同领域的调控机制与cAMP信号通路联系起来的下游信号调控因子；另一方面，对于生长发育、有性/无性生殖、次生代谢以及致病性等方面的调控机制还有待完善。因此，对于cAMP信号通路对下游的组分及调控机制的研究，可能是未来深入了解植物病原真菌的切口，可为今后防控不同植物病原真菌提供新的抑菌药物靶点，同时也为未来控制植物病原真菌侵染提供新的科学依据。

基金

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温州市科研项目(N20240006)
温州市科技项目(X2023104)
浙江省农科院专项(2024XJXK03)
浙江省农科院专项(2024R26CB002)
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2024年第64卷第12期

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doi: 10.13343/j.cnki.wsxb.20240405

接收时间：2024-07-01
首发时间：2026-03-21
出版时间：2024-09-24

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收稿日期：2024-07-01
录用日期：2024-09-19

基金

Wenzhou Scientific Research Project(N20240006)

温州市科研项目(N20240006)

Wenzhou Science and Technology Project(X2023104)

温州市科技项目(X2023104)

Special Funding Project of Zhejiang Academy of Agricultural Sciences(2024XJXK03)

浙江省农科院专项(2024XJXK03)

Special Funding Project of Zhejiang Academy of Agricultural Sciences(2024R26CB002)

浙江省农科院专项(2024R26CB002)

Industrial Technology Service Team Project of Ouhai Science and Technology Innovation Center, Zhejiang Academy of Agricultural Sciences

浙江省农业科学院瓯海科创中心产业科技服务团项目

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浙江省亚热带作物研究所, 浙江温州 325005

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2种不同金属材料的力学参数

科 Family	属数 Number of genus	种数 Number of species	占总种数比例 Percentage of total species (%)	属 Genus	种数 Number of species	占总种数比例 Percentage of total species (%)
鹅膏菌科Amanitaceae	2	11	5.26	鹅膏菌属 Amanita	10	4.78
小菇科 Mycenaceae	2	12	5.74	丝盖伞属 Inocybe	5	2.39
多孔菌科 Polyporaceae	8	14	6.70	蜡蘑属 Laccaria	5	2.39
红菇科 Russulaceae	3	23	11.00	小皮伞属 Marasmius	6	2.87
				小菇属 Mycena	11	5.26
				光柄菇属 Pluteus	5	2.39
				红菇属 Russula	17	8.13
				栓菌属 Trametes	5	2.39

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Fungus	Function	References
Sclerotinia sclerotiorum	Mycelial and sclerotium development, pathogenicity	[55]
Fusarium fujikuroi	Mycelial development, conidia and carotenoids production	[56]
Fusarium proliferatum	Mycelial and sclerotium development, pathogenicity	[57]
Fusarium verticillioides	Mycelial and sclerotium development, pathogenicity, coercion tolerance	[58]
Metarhizium acridum	Mycelial development, pathogenicity, coercion tolerance	[16]
Beauveria bassiana	Mycelial development, conidia production, pathogenicity, coercion tolerance	[59]
Aspergillus flavus	Mycelial development, conidia, sclerotium and toxin production, pathogenicity, coercion tolerance	[60]
Penicillium digitatum	Mycelial development, conidial production and germination, pathogenicity	[61]
Colletotrichum higginsianum	Mycelial development, conidia production, pathogenicity, coercion tolerance	[62]

Fungus

Function

References

Sclerotinia sclerotiorum

Mycelial and sclerotium development, pathogenicity

[55]

Fusarium fujikuroi

Mycelial development, conidia and carotenoids production

[56]

Fusarium proliferatum

Mycelial and sclerotium development, pathogenicity

[57]

Fusarium verticillioides

Mycelial and sclerotium development, pathogenicity, coercion tolerance

[58]

Metarhizium acridum

Mycelial development, pathogenicity, coercion tolerance

[16]

Beauveria bassiana

Mycelial development, conidia production, pathogenicity, coercion tolerance

[59]

Aspergillus flavus

Mycelial development, conidia, sclerotium and toxin production, pathogenicity, coercion tolerance

[60]

Penicillium digitatum

Mycelial development, conidial production and germination, pathogenicity

[61]

Colletotrichum higginsianum

Mycelial development, conidia production, pathogenicity, coercion tolerance

[62]

Fungus	PKA	Function	References
Sclerotinia sclerotiorum	SsPKA	Mycelial development, pathogenicity, autophagy	[63]
SsPKAR	Mycelial development, pathogenicity, autophagy, infection cushion and sclerotium formation
Fusarium fujikuroi	FfPKA1	Mycelial development, bicarbacin prodcution	[64]
FfPKA2	Mycelial development, gibberellin (GA) synthesis
Fusarium verticillioides	CPK1	Mycelial development, conidia production, pathogenicity	[65]
Colletotrichum trifolii-alfalfa	Ct-PKAC	Mycelial development, conidia production, infection cushion formation, pathogenicity, coercion tolerance	[66]
Colletotrichum orbiculare-cucumber	Co-Rpk1	Mycelial development, conidia production, pathogenicity	[67]
Co-Cpk1	Conidia germination, infection cushion function, pathogenicity
Colletotrichum gloeosporioides-mango	Cg-PKAC	Conidia production, infection cushion function, pathogenicity	[68]
Colletotrichum higginsianum-Arabidopsis	Ch-PKA1	Mycelial development, conidia production, infection cushion formation, stress response, pathogenicity	[69]

Fungus

PKA

Function

References

Sclerotinia sclerotiorum

SsPKA

Mycelial development, pathogenicity, autophagy

[63]

SsPKAR

Mycelial development, pathogenicity, autophagy, infection cushion and sclerotium formation

Fusarium fujikuroi

FfPKA1